DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils

Abstract

Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallophores within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrices. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) of soils from native tallgrass prairies in Kansas and Iowa. Both plant and fungal metallophores were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant Fe acquisition and homeostasis, including mugineic acids,more » deoxymugineic acid, nicotianamine, and hydroxynicotianamines, dominated the speciation of divalent metals such as Ni, Cu, and Zn (2–90 pmol/g soil). In contrast, the fungal siderophore ferricrocin was specific for trivalent Fe (7–32 pmol/g soil). These results define biochemical pathways that underpin the regulation of metals in the grassland rhizosphere. They also raise new questions about the competition of these compounds for metal binding and their bioavailability to different members of the rhizosphere population. In conclusion, small structural modifications result in significant differences in metal ligand selectivity, and likely impact metal uptake within the rhizosphere of grassland soils.« less

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [2]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Earth and Biological Sciences Directorate
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1427526
Alternate Identifier(s):
OSTI ID: 1548618
Report Number(s):
PNNL-SA-128577
Journal ID: ISSN 0038-0717; PII: S0038071718300671
Grant/Contract Number:  
AC05-76RL01830; 49644
Resource Type:
Accepted Manuscript
Journal Name:
Soil Biology and Biochemistry
Additional Journal Information:
Journal Volume: 120; Journal Issue: C; Journal ID: ISSN 0038-0717
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Phytosiderophores; Hydroxamates; Metal exchange; High resolution mass spectrometry; Soil microbiome

Citation Formats

Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States: N. p., 2018. Web. doi:10.1016/j.soilbio.2018.02.018.
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., & Jansson, Janet K. Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils. United States. https://doi.org/10.1016/j.soilbio.2018.02.018
Boiteau, Rene M., Shaw, Jared B., Pasa-Tolic, Ljiljana, Koppenaal, David W., and Jansson, Janet K. Thu . "Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils". United States. https://doi.org/10.1016/j.soilbio.2018.02.018. https://www.osti.gov/servlets/purl/1427526.
@article{osti_1427526,
title = {Micronutrient metal speciation is controlled by competitive organic chelation in grassland soils},
author = {Boiteau, Rene M. and Shaw, Jared B. and Pasa-Tolic, Ljiljana and Koppenaal, David W. and Jansson, Janet K.},
abstractNote = {Many elements are scarcely soluble in aqueous conditions found in high pH environments, such as calcareous grassland soils, unless complexed to strong binding organic ligands. To overcome this limitation, some plants and microbes produce chelators that solubilize micronutrient metals such as Fe, Ni, Cu, and Zn from mineral phases. These complexes are taken up by organisms via specific membrane receptors, thereby differentially impacting the bioavailability of these metals to the plant and microbial community. Although the importance of these chelation strategies for individual organisms has been well established, little is known about which pathways coexist within rhizosphere microbiomes or how they interact and compete for metal binding. Identifying these metallophores within natural ecosystems has remained a formidable analytical challenge due to the vast diversity of compounds and poorly defined metabolic processes in complex soil matrices. Herein, we employed recently developed liquid chromatography (LC) mass spectrometry (MS) methods to characterize the speciation of water-soluble dissolved trace elements (Fe, Ni, Cu, and Zn) of soils from native tallgrass prairies in Kansas and Iowa. Both plant and fungal metallophores were identified, revealing compound-specific patterns of chelation to biologically essential metals. Numerous metabolites typically implicated in plant Fe acquisition and homeostasis, including mugineic acids, deoxymugineic acid, nicotianamine, and hydroxynicotianamines, dominated the speciation of divalent metals such as Ni, Cu, and Zn (2–90 pmol/g soil). In contrast, the fungal siderophore ferricrocin was specific for trivalent Fe (7–32 pmol/g soil). These results define biochemical pathways that underpin the regulation of metals in the grassland rhizosphere. They also raise new questions about the competition of these compounds for metal binding and their bioavailability to different members of the rhizosphere population. In conclusion, small structural modifications result in significant differences in metal ligand selectivity, and likely impact metal uptake within the rhizosphere of grassland soils.},
doi = {10.1016/j.soilbio.2018.02.018},
journal = {Soil Biology and Biochemistry},
number = C,
volume = 120,
place = {United States},
year = {Thu Mar 08 00:00:00 EST 2018},
month = {Thu Mar 08 00:00:00 EST 2018}
}

Journal Article:

Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

Figures / Tables:

Figure 1 Figure 1: Plant phytosiderophores and fungal siderophores identified from grassland prairie soils in this study.

Save / Share:

Works referenced in this record:

Ecology of siderophores with special reference to the fungi
journal, January 2007


Siderophores and the Dissolution of Iron-Bearing Minerals in Marine Systems
journal, January 2005


Ferricrocin functions as the main intracellular iron-storage compound in mycelia ofNeurospora crassa
journal, January 1988

  • Matzanke, Berthold F.; Bill, Eckard; Trautwein, Alfred X.
  • Biology of Metals, Vol. 1, Issue 1
  • DOI: 10.1007/BF01128013

Retention of phytosiderophores by the soil solid phase – adsorption and desorption
journal, February 2016


Geochemical Processes Constraining Iron Uptake in Strategy II Fe Acquisition
journal, October 2014

  • Schenkeveld, W. D. C.; Schindlegger, Y.; Oburger, E.
  • Environmental Science & Technology, Vol. 48, Issue 21
  • DOI: 10.1021/es5031728

Siderophores in environmental research: roles and applications: Siderophores in environmental research
journal, February 2014


Root exudation of phytosiderophores from soil‐grown wheat
journal, June 2014

  • Oburger, Eva; Gruber, Barbara; Schindlegger, Yvonne
  • New Phytologist, Vol. 203, Issue 4
  • DOI: 10.1111/nph.12868

Structural biology of bacterial iron uptake
journal, September 2008

  • Krewulak, Karla D.; Vogel, Hans J.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 9
  • DOI: 10.1016/j.bbamem.2007.07.026

Competition between micro‐organisms and roots of barley and sorghum for iron accumulated in the root apoplasm
journal, August 1995


Molecular aspects of Cu, Fe and Zn homeostasis in plants
journal, July 2006

  • Grotz, Natasha; Guerinot, Mary Lou
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1763, Issue 7
  • DOI: 10.1016/j.bbamcr.2006.05.014

Relationships between Soybean Yield, Soil pH, and Soil Carbonate Concentration
journal, July 2007

  • Rogovska, Natalia P.; Blackmer, Alfred M.; Mallarino, Antonio P.
  • Soil Science Society of America Journal, Vol. 71, Issue 4
  • DOI: 10.2136/sssaj2006.0235

Siderophores in forest soil solution
journal, November 2004

  • Holmstr�m, Sara J. M.; Lundstr�m, Ulla S.; Finlay, Roger D.
  • Biogeochemistry, Vol. 71, Issue 2
  • DOI: 10.1007/s10533-004-9915-5

Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes
journal, June 2009


Mining iron: Iron uptake and transport in plants
journal, April 2007


An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS
journal, January 2015

  • Boiteau, Rene M.; Repeta, Daniel J.
  • Metallomics, Vol. 7, Issue 5
  • DOI: 10.1039/C5MT00005J

Siderophore Utilization by Bradyrhizobium japonicum
journal, May 1993


Detection and identification of ferricrocin produced by ectendomycorrhizal fungi in the genusWilcoxina
journal, July 1996

  • Prabhu, Vikram; Biolchini, Peter F.; Boyer, Gregory L.
  • BioMetals, Vol. 9, Issue 3
  • DOI: 10.1007/BF00817920

Synthesis and properties of different metal complexes of the siderophore desferriferricrocin
journal, February 2005


An Extracellular Siderophore Is Required to Maintain the Mutualistic Interaction of Epichloë festucae with Lolium perenne
journal, May 2013


An Iron Uptake Operon Required for Proper Nodule Development in the Bradyrhizobium japonicum -Soybean Symbiosis
journal, September 2005

  • Benson, Heather P.; Boncompagni, Eric; Guerinot, Mary Lou
  • Molecular Plant-Microbe Interactions®, Vol. 18, Issue 9
  • DOI: 10.1094/MPMI-18-0950

A cross-platform toolkit for mass spectrometry and proteomics
journal, October 2012

  • Chambers, Matthew C.; Maclean, Brendan; Burke, Robert
  • Nature Biotechnology, Vol. 30, Issue 10
  • DOI: 10.1038/nbt.2377

Detection of Iron Ligands in Seawater and Marine Cyanobacteria Cultures by High-Performance Liquid Chromatography–Inductively Coupled Plasma-Mass Spectrometry
journal, April 2013

  • Boiteau, Rene M.; Fitzsimmons, Jessica N.; Repeta, Daniel J.
  • Analytical Chemistry, Vol. 85, Issue 9
  • DOI: 10.1021/ac3034568

Microbial Iron Acquisition: Marine and Terrestrial Siderophores
journal, October 2009

  • Sandy, Moriah; Butler, Alison
  • Chemical Reviews, Vol. 109, Issue 10
  • DOI: 10.1021/cr9002787

Vertical distribution of fungal communities in tallgrass prairie soil
journal, September 2010

  • Jumpponen, Ari; Jones, Kenneth L.; Blair, John
  • Mycologia, Vol. 102, Issue 5
  • DOI: 10.3852/09-316

Review on iron availability in soil: interaction of Fe minerals, plants, and microbes
journal, November 2013

  • Colombo, Claudio; Palumbo, Giuseppe; He, Ji-Zheng
  • Journal of Soils and Sediments, Vol. 14, Issue 3
  • DOI: 10.1007/s11368-013-0814-z

Moleculo Long-Read Sequencing Facilitates Assembly and Genomic Binning from Complex Soil Metagenomes
journal, June 2016


The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake
journal, January 2015


Iron utilization and metabolism in plants
journal, June 2007

  • Briat, Jean-François; Curie, Catherine; Gaymard, Frédéric
  • Current Opinion in Plant Biology, Vol. 10, Issue 3
  • DOI: 10.1016/j.pbi.2007.04.003

Trace metal transport by marine microorganisms: implications of metal coordination kinetics
journal, January 1993

  • Hudson, Robert J. M.; Morel, François M. M.
  • Deep Sea Research Part I: Oceanographic Research Papers, Vol. 40, Issue 1
  • DOI: 10.1016/0967-0637(93)90057-A

Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores
journal, April 1990


The effect of soil horizon and mineral type on the distribution of siderophores in soil
journal, April 2014


Nitrogen fertilization increases diversity and productivity of prairie communities used for bioenergy
journal, June 2012


Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis
journal, June 2001


Functional group and fertilization affect the composition and bioenergy yields of prairie plants
journal, May 2012


Iron oxide dissolution and solubility in the presence of siderophores
journal, March 2004


Tallgrass prairie soil fungal communities are resilient to climate change
journal, August 2014


Coordination chemistry of microbial iron transport compounds. 24. Characterization of coprogen and ferricrocin, two ferric hydroxamate siderophores
journal, February 1983

  • Wong, Geoffrey B.; Kappel, Mary J.; Raymond, Kenneth N.
  • Journal of the American Chemical Society, Vol. 105, Issue 4
  • DOI: 10.1021/ja00342a027

Quantification of Hydroxamate Siderophores in Soil Solutions of Podzolic Soil Profiles in Sweden
journal, June 2006


Iron Uptake and Transport in Plants: The Good, the Bad, and the Ionome
journal, October 2009

  • Morrissey, Joe; Guerinot, Mary Lou
  • Chemical Reviews, Vol. 109, Issue 10
  • DOI: 10.1021/cr900112r

Root-Secreted Nicotianamine from Arabidopsis halleri Facilitates Zinc Hypertolerance by Regulating Zinc Bioavailability
journal, August 2014


Hydroxylated Phytosiderophore Species Possess an Enhanced Chelate Stability and Affinity for Iron(III)
journal, November 2000

  • von Wirén, Nicolaus; Khodr, Hicham; Hider, Robert C.
  • Plant Physiology, Vol. 124, Issue 3
  • DOI: 10.1104/pp.124.3.1149

Chemistry and biology of siderophores
journal, January 2010

  • Hider, Robert C.; Kong, Xiaole
  • Natural Product Reports, Vol. 27, Issue 5
  • DOI: 10.1039/b906679a

Sustainable bioenergy production from marginal lands in the US Midwest
journal, January 2013

  • Gelfand, Ilya; Sahajpal, Ritvik; Zhang, Xuesong
  • Nature, Vol. 493, Issue 7433
  • DOI: 10.1038/nature11811

ZmYS1 Functions as a Proton-coupled Symporter for Phytosiderophore- and Nicotianamine-chelated Metals
journal, March 2004

  • Schaaf, Gabriel; Ludewig, Uwe; Erenoglu, Bülent E.
  • Journal of Biological Chemistry, Vol. 279, Issue 10
  • DOI: 10.1074/jbc.M311799200

Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake
journal, January 2001

  • Curie, Catherine; Panaviene, Zivile; Loulergue, Clarisse
  • Nature, Vol. 409, Issue 6818
  • DOI: 10.1038/35053080

Trace metal levels in edible wild fungi
journal, December 2012

  • Severoglu, Z.; Sumer, S.; Yalcin, B.
  • International Journal of Environmental Science and Technology, Vol. 10, Issue 2
  • DOI: 10.1007/s13762-012-0139-2

Acquisition, Transport, and Storage of Iron by Pathogenic Fungi
journal, July 1999


Kinetic studies on the specificity of chelate-iron uptake in Aspergillus
journal, September 1975


Stabilities of Metal Complexes of Mugineic Acids and Their Specific Affinities for Iron(III)
journal, December 1989

  • Murakami, Tasuku; Ise, Kunio; Hayakawa, Minato
  • Chemistry Letters, Vol. 18, Issue 12
  • DOI: 10.1246/cl.1989.2137

Equilibrium and kinetic modelling of the dynamic rhizosphere
journal, December 2014


A specific transporter for iron(III)-phytosiderophore in barley roots
journal, May 2006


Facing the challenges of Cu, Fe and Zn homeostasis in plants
journal, April 2009

  • Palmer, Christine M.; Guerinot, Mary Lou
  • Nature Chemical Biology, Vol. 5, Issue 5
  • DOI: 10.1038/nchembio.166

Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean
journal, December 2016

  • Boiteau, Rene M.; Mende, Daniel R.; Hawco, Nicholas J.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 50
  • DOI: 10.1073/pnas.1608594113

Fungal siderophore metabolism with a focus on Aspergillus fumigatus
journal, January 2014


Works referencing / citing this record:

Effects of calcium on the kinetics of a model disjunctive ligand exchange reaction: implications for dynamic trace metal ion speciation
journal, January 2019

  • Rea, Laura T.; Xu, Yi; Boland, Nathan E.
  • Environmental Science: Processes & Impacts, Vol. 21, Issue 1
  • DOI: 10.1039/c8em00301g

Siderophore profiling of co-habitating soil bacteria by ultra-high resolution mass spectrometry
journal, January 2019

  • Boiteau, Rene M.; Fansler, Sarah J.; Farris, Yuliya
  • Metallomics, Vol. 11, Issue 1
  • DOI: 10.1039/c8mt00252e

The kinetics of siderophore‐mediated olivine dissolution
journal, February 2019

  • Torres, Mark A.; Dong, Sijia; Nealson, Kenneth H.
  • Geobiology, Vol. 17, Issue 4
  • DOI: 10.1111/gbi.12332

How Plants Handle Trivalent (+3) Elements
journal, August 2019

  • Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
  • International Journal of Molecular Sciences, Vol. 20, Issue 16
  • DOI: 10.3390/ijms20163984

How Plants Handle Trivalent (+3) Elements
journal, August 2019

  • Poschenrieder, Charlotte; Busoms, Silvia; Barceló, Juan
  • International Journal of Molecular Sciences, Vol. 20, Issue 16
  • DOI: 10.3390/ijms20163984

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.